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Seasonality of Old World Screwworm Myiasis in the Mesopotamia Valley in Iraq

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Seasonality of Old World Screwworm Myiasis in the Mesopotamia Valley in Iraq Medical and Veterinary Entomology (2005) 19, 140–150 Seasonality of Old World screwworm myiasis in the Mesopotamia valley in Iraq A. SIDDIG1 , S. AL JOWARY2 , M. AL IZZI3 , J. HOPKINS4 ,M.J.R.HALL5 and J. SLINGENBERGH4 1Ministry of Science and Technology, Khartoum, Sudan, 2College of Education for Women, University of Baghdad, Baghdad, Iraq, 3Entomology Department, Iraqi Atomic Energy Commission, Ministry of Science and Technology, Baghdad, Iraq, 4Animal Health Division, Food and Agriculture Organization of the United Nations, Rome, Italy and 5The Natural History Museum, London, U.K. Abstract. Following the first recorded introduction of the Old World screwworm fly (OWS), Chrysomya bezziana Villeneuve (Diptera: Calliphoridae), into the Mesopotamia valley in Iraq in September 1996, cases of livestock myiasis caused by OWS developed a distinctly seasonal pattern. The annual cycle of clinical OWS cases is explained here on the basis of environmental variables that affect the different life-cycle stages of C. bezziana. This analysis suggests that low tempera- tures restricted pupal development during the winter, whereas the dispersal of adult flies was constrained by hot/dry summer conditions. A restricted number of OWS foci persisted throughout the year. In these foci, pupal development was fastest during the autumn months. In autumn, rapid multiplication, lasting several OWS generations, allowed subsequent adult fly dispersal across the valley floor during the winter. Hence, the monthly incidence of clinical OWS cases in livestock peaked during December–January and was lowest during July–August. In addi- tion to temperature and humidity, vegetation cover played a role in OWS dis- tribution. Hence the majority of OWS cases were clustered in the medium density type of vegetation [normalized difference vegetation index (NDVI) values of 0.2–0.4] along the main watercourses in the marshy Mesopotamia valley. Although sheep were the host most commonly infested by C. bezziana, local sheep density was not found to be a major factor in disease spread. Satellite imagery and the application of Geographical Information System (GIS) tools were found to be valuable in understanding the distribution of OWS in relation to vegetation and watercourses. The presence of screwworm in Iraq, at the perimeter of the intercontinental OWS distribution, may give rise to major seasonal flare-ups. Key words. Chrysomya bezziana, geographical information system, myiasis, Old World screwworm, seasonality, sheep, Iraq. Introduction fly (NWS), Cochliomyia hominivorax Coquerel, have a very similar biology, ecology and behaviour (Spradbery, 1994) Although classified in different genera of the blowfly family, and both species are obligate parasites of vertebrates in Calliphoridae, the Old World screwworm fly (OWS), Chry- their larval stages, causing traumatic myiasis. There is no somya bezziana Villeneuve, and the New World screwworm overlap in their geographical distributions. NWS is con- fined to the Americas, but OWS is found across sub- Saharan Africa, the Indian subcontinent, South-east Asia, Correspondence: Dr Awatif Siddig, Ministry of Science and and the Gulf region of the Arabian Peninsula (Norris & Technology, Animal Resources Research Corporation, 6 Street no. Murray, 1964). Molecular analysis of OWS populations 1 Al Amarat, Khartoum, Sudan. Tel: +24 99 1269 4430; fax: from sub-Saharan Africa, the Gulf region and Asia suggests 24 91 8347 2690; E-mail: [email protected] that the geographical isolation of the sub-Saharan African 140 # 2005 The Royal Entomological Society Old World screwworm in Iraq 141 and Asian lineages of C. bezziana took place about one More permanent infestations appear to have occurred in million years ago (Hall et al., 2001). This static distribution the Sultanate of Oman and in Iraq. A 10-month survey pattern is surprising given that domestic livestock have carried out in the Sultanate of Oman during 1989–1990 replaced wild ungulates as the most commonly infested found 82 OWS cases in the northern part of the country host animals throughout most of the geographical range during the cooler months of the year (Spradbery et al., of OWS. Livestock numbers across the world are on the 1992). The first introduction of OWS into Iraq reportedly increase and so is the annual trade in live animals (FAO- took place in June 1996 (Abdul Rassoul et al., 1996). STAT, 2001). It may be expected that further spread of Traumatic myiasis assumed epidemic proportions during livestock will occur and, with them, there is the potential the winter months of late 1996 and early 1997 (Hopkins & for spread of parasites and pathogens. Khattat, 1997), ultimately giving rise to 9306 and 45 398 The Middle East region is an area of particular interest, cases in 1996 and 1997, respectively (Al-Adhadh, 2001). with extensive livestock movement. It has been suggested Scarcity of insecticide limited effective disease control and that the isolation of African and Asian OWS lineages is a second epidemic wave developed during the second maintained by the zone of unfavourable arid environments winter, with a monthly incidence amounting to 23 000 between the Gulf and sub-Saharan Africa (Hall et al., 2001). OWS clinical cases in December 1997 (Al-Izzi et al., Even so, it remains unclear why African lineage OWS have 1999a). During 1998, significant quantities of insecticide so far not been detected in the Arabian Peninsula given that became available to the veterinary clinics and the incidence millions of live ruminants are imported every year from the was eventually reduced. The objective of the present study Greater Horn of Africa. Also difficult to explain is the fact was to examine the interaction of environmental factors and that screwworm flies have not become established in fly biology that gave rise to the observed seasonality of Australia, despite the presence of OWS in Papua New OWS myiasis cases. Guinea and the occasional detection of dead C. bezziana flies in light fittings on livestock vessels returning from the Gulf area or on-board commercial aircraft arriving from OWS-infested India (Rajapaksa & Spradbery, 1989). Materials and methods Although the global OWS and NWS picture has remained relatively unchanged, there has been considerable Collection of case data local spread, particularly at the perimeter of the continental OWS and NWS fly distributions. Outbreaks of NWS In September 1996, the presence of OWS in Iraq was myiasis occurred in the United States during the 1930 s, confirmed by the FAO Collaborating Centre on Myiasis reaching Florida and then the south-eastern states in 1933 Causing Insects and their Identification at the Natural His- and extending up to the great lakes in 1935 (Readshaw, tory Museum in London, U.K. (Hall, 1997). Subsequently, 1986). Mild winters and moist summers supported the strict guidelines were issued to field veterinary services and widespread persistence of NWS, until its eradication by clinics on how to record any clinical cases of traumatic the Sterile Insect Technique (SIT) (Wyss, 2001). A shipment myiasis in livestock, detailing host species, breed, age and of NWS-affected livestock is believed to have brought locality for each case encountered. Medical centres received C. hominivorax from the Americas to northern Libya in instructions for the recording of human cases. 1988 (Gabaj et al., 1989; Lindquist et al., 1992). Here also, Field data were collated bimonthly and the findings SIT was applied to eradicate the incursion (FAO, 1992). reported to relevant national, regional and international The success of the SIT campaign was probably enhanced organizations. Clinical cases of traumatic myiasis caused by low winter temperatures in both the Southern United by C. bezziana were identified and recorded by veterinarians States (Readshaw, 1986) and Libya (Krafsur & Lindquist, in a network of 111 government veterinary clinics (Al-Ani, 1996). 1997; Al-Taweel et al., 2000), which were geo-referenced for In 1983, an accidental introduction of C. bezziana from a the production of digital maps. Identifications were based ship reportedly took place in the coastal Salalah area of the on the descriptions given by Zumpt (1965) and Spradbery Sultanate of Oman (Spradbery et al., 1992). A total of (1991) and sub-samples were confirmed by the 10 500 animals became affected until the situation was Natural History Museum in Baghdad. They are believed finally brought in check by insecticide treatments. Similarly, to present an accurate record of OWS cases because C. bezziana spread out from the Gulf port of Booshehr, this species was the only one in the region responsible Iran, in April 1995 (Navidpour et al., 1996; Haddadzadeh for the deeply penetrating wounds characteristic of et al., 1997), prompting a major insecticidal campaign. screwworm species. Wohlfahrtia magnifica (Diptera: Minor incursions have also occurred in other Gulf States, Sarcophagidae), which produces similar wounds, is also including an introduction of C. bezziana into Bahrain in found in Iraq, but only in the northern regions and not 1977 (Kloft et al., 1981) and into the United Arab Emirates in cases reported here. The monthly incidences of OWS in in 1988 (Spradbery & Kirk, 1992). Sporadic cases of OWS livestock considered here were just those recorded for the myiasis also occur in Saudi Arabia, in humans (Ansari & first 2 years following OWS introduction. Subsequently the Oertley, 1982) and livestock (Alahmed, 2002; El-Azazy & use of insecticides increased, distorting
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